Science of the Total Environment 408 (2010) 2155–2162

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Accumulation of polychlorinated biphenyls and brominated flame retardants inbreast milk from women living in Vietnamese e-waste recycling sites

Nguyen Minh Tue a, Agus Sudaryanto b, Tu Binh Minh c, Tomohiko Isobe b, Shin Takahashi a,⁎,Pham Hung Viet c, Shinsuke Tanabe a

a Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japanb Senior Research Fellow Center, Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japanc Centre for Environmental Technology and Sustainable Development, Hanoi University of Science, 334 Nguyen Trai, Hanoi, Vietnam

⁎ Corresponding author. Tel./fax: +81 89 927 8196.E-mail address: shint@agr.ehime-u.ac.jp (S. Takahas

0048-9697/$ – see front matter © 2010 Elsevier B.V. Aldoi:10.1016/j.scitotenv.2010.01.012

a b s t r a c t

a r t i c l e i n f o

Article history:Received 28 October 2009Received in revised form 6 January 2010Accepted 8 January 2010Available online 8 February 2010

Keywords:Breast milkE-wasteExposure pathwayHBCDPBDEPCB

This study investigated the contamination status of PCBs, PBDEs and HBCDs in human and possible exposurepathways in three Vietnamese e-waste recycling sites: Trang Minh (suburb of Hai Phong city), Dong Mai andBui Dau (Hung Yen province), and one reference site (capital city Hanoi) by analysing human breast milksamples and examining the relationships between contaminant levels and lifestyle factors. Levels of PBDEs,but not PCBs and HBCDs, were significantly higher in Trang Minh and Bui Dau than in the reference site. Therecyclers from Bui Dau had the highest levels of PBDEs (20–250 ng g−1 lipid wt.), higher than in thereference group by two orders of magnitude and more abundant than PCBs (28–59 ng g−1 lipid wt.), andwere also the only group with significant exposure to HBCDs (1.4–7.6 ng g−1 lipid wt.). A specific accu-mulation, unrelated to diet, of low-chlorinated PCBs and high-brominated PBDEs was observed in e-wasterecyclers, suggesting extensive exposure to these compounds during e-waste recycling activities, possiblythrough inhalation and ingestion of dust. The estimated infant intake dose of PBDEs from breast milk of somemothers occupationally involved in e-waste recycling were close to or higher than the reference doses issuedby the U.S. EPA.

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1. Introduction

Waste electrical and electronic equipment, also known as e-waste,refers to end-of-life products encompassing information-communi-cationdevices, consumer electronics andhousehold appliances. Owingto the short life span of devices such as computers, television sets,stereo systems, printers and cell phones, e-waste is generated in largeamounts, with an annual volume of 20–50 million tonnes world-wideand increases rapidly at a rate of 3–5% per year (UNEP, 2005). Thehazard of e-waste lies in the high content of many toxic substances(BAN and SVCT, 2002) including heavy metals (lead, mercury,cadmium, etc.) and persistent organohalogen compounds such aspolychlorinated biphenyls (PCBs) and brominated flame retardants(BFRs). PCBs are present in older electrical capacitors and transformersas coolants and dielectrics whereas BFRs are additives found in mostpolymeric parts (printed circuit boards, cable coatings, plastic casings,etc.). There are increasing evidences that BFRs, such as polybromi-nated diphenyl ethers (PBDEs) and hexabromocyclododecanes(HBCDs), exhibit a range of toxic effects similar to PCBs, including

endocrine disruption aswell as reproductive and neurodevelopmentaltoxicity (Legler and Brouwer, 2003; Birnbaum and Staskal, 2004).

Uncontrolled e-waste recycling has become a topic of seriousconcern in recent years. It is estimated that up to 80% of e-waste fromindustrialised countries is exported to Asian developing countries forrecycling, exploiting the inexpensive cost of labour and weakenforcement of environmental laws (BAN and SVCT, 2002). Largescale waste processing operations employing primitive practices suchas uncontrolled dismantling, acid stripping and open burning inChinese e-waste recycling sites (EWRSs) have resulted in severeenvironmental contamination (Wong et al., 2007). The humanexposure levels to PCBs in Taizhou region (Zhao et al., 2007) and toPBDEs in Guiyu town (Bi et al., 2007) are two of the highest everreported. In other Asian developing countries such as Cambodia, India,Philippines and Viet Nam, although open waste disposal sites havebeen identified as potential sources of PCBs and dioxin-like com-pounds (Minh et al., 2003), information on EWRS are lacking. Avail-able data, albeit limited, indicate that the levels of PCBs and BFRs inthe general populations from these countries are lower than thosefrom developed countries (Schecter et al., 2004; Sudaryanto et al.,2005, 2008a; Malarvannan et al., 2009); nevertheless EWRSs aresuspected as potential hotspots of these contaminants. In this context,the present study was carried out to assess the human exposure topersistent organohalogen compounds related to e-waste recycling in

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Viet Nam. Breast milk was selected as bioindicator on account of thesimple and non-invasive sampling, relatively high content of lipid andlipophilic contaminants, and relevance to infants' health. PCBs, PBDEsand HBCDs were determined in human breast milk collected fromthree EWRSs and a reference site in view of contamination levels,congener patterns, influence of lifestyle factors and potential healthrisk for breastfeeding infants.

2. Materials and methods

2.1. Study locations

End-of-life electrical and electronic equipment in Viet Nam areoften picked up by scrap collectors, through purchase from theirformer owners or by scavenging domestic waste disposal sites. Thewastes are then transported to trade villages specialised in recycling.The present study investigated three e-waste recycling sites located inthe Red River delta region, in the northern part of the country; DongMai (DM, Hung Yen province, battery recycling), Trang Minh (TM,suburb of Hai Phong City, e-waste dismantling) and Bui Dau (BD,Hung Yen province, e-waste dismantling). All study locations weresmall villages with approximately 80 households or less. E-wasterecycling as a trade started in these villages very recently at thebeginning of the decade, except in the case of DMwhere the recyclingof lead from batteries has been occurring for almost four decades.Most businesses are family-based and e-waste is recycled in thebackyard of the house. The waste processing often consists of onlydismantling, retrieval of easily accessible metals and grinding plasticcasings intro reusable pellets. Circuit boards are not processed andinstead sold to foreign buyers. Alongside these recent recyclingactivities, the villages still maintain traditional crop production. Aminority of the families also raise livestock or aqua-culture fish inlimited quantities in-house, but the main supplies of livestockproduces and fish for all the three communities are from theneighbouring communes.

2.2. Sample collection

The sampling survey was conducted in August 2007. In each of thethree recycling sites, the number of nursing mothers was limited toaround 20 or less. Four breast milk samples from DM, eleven from TMand nine from BD were collected from the mothers who agreed todonate. As reference, another nine samples were collected from thecapital Hanoi (HN), a typical urban area. Informed consents wereobtained from all donors. Questionnaire survey was also conducted toacquire personal information on age, height and weight measure-ments, number of deliveries and duration of nursing periods,occupation (recyclers or non-recyclers), period of involvement inrecycling activities and dietary habit (Table 1). All donors were non-smokers and appeared healthy. Breast milk was expressed by thedonor or with the help of a midwife into a solvent-precleaned glasscontainer with Teflon-lined screw caps. The samples were kept ingel ice immediately after collection and then sent within 8 h to our

Table 1General characteristics of the donors of breast milk.

Parameters Hanoi (n=9) Dong M

Age (year) 23–35 (28.2) 25–31Weight (kg) 46–62 (54.3) 42–52Height (cm) 155–167 (160.9) 153–15Body mass index (kg m−2) 16.5–25.4 (21.1) 17.9–21Number of children 1–2 (1.67) 1–4 (2.Total nursing time (month) 4.5–25 (12) 4–57 (2Occupation 89% office worker 25% rec

11% housewife 75% far

Values between parentheses are arithmetic means.

laboratory in Viet Nam and frozen at−20 °C. Later the frozen sampleswere air-transported with gel ice to the Environmental SpecimenBank (es-BANK, Ehime University, Japan) and stored at −25 °C inuntil analysis.

2.3. Chemical analyses

Approximately 40 g of sample was freeze-dried and then Soxhlet-extracted with 300 ml diethyl ether and 100 ml hexane for 7 h. About10% of the extract was used for determination of the lipid contentusing the gravimetric method. The remaining extract was spiked with13C12–PCBs, 13C12–PBDEs (5 ng each) and 13C12–HBCDs (10 ng each)as standard surrogates, subjected to gel permeation chromatography(packed Bio-Bead S-X 3, Bio-Rad Laboratories, USA) for lipid removalusing a hexane/dichloromethane (DCM) mixture (1:1 v/v) as eluant.The cleaned-up extract was then concentrated and passed through 4 gof activated silica gel (Wakogel® DX, Wako, USA) packed in a glasscolumn for separation of HBCDs from PCBs and PBDEs. The firstfraction containing PCBs and PBDEs, eluted with a mixture of hexane/DCM (95:5 v/v, 80 ml), was spiked with 5 ng 13C12–BDE-139 asinternal standard and solvent-exchanged into iso-octane. The HBCDfraction, eluted with another mixture of hexane/DCM (75:25 v/v,100 ml), was concentrated until dryness and then redissolved in amethanol solution containing deuterium-labelled HBCDs-d18 (10 ngeach) as internal standards.

PCBs (62 congeners) and PBDEs (14 congeners commonly found inabundance in the technical PBDE mixtures (La Guardia et al., 2006),namely BDE-3, -15, -28, -47, -99, -100, -153, -154, -183, -196, -197,-206, -207, and -209) were quantified using a gas chromatograph(Agilent 7890 series) equipped with a mass-selective detector(Agilent 5975 series) and a DB-1 fused silica column (J&W Scientific)having 0.25 mm i.d.×30 m×0.25 µm film thickness for PCBs andmono- to hepta-BDEs or 0.25 mm i.d.×15 m×0.1 µm film thicknessfor octa- to deca-BDEs. The GC oven temperature program for PCBswas: from 120 °C to 180 °C at 20 °C min−1, 2 °C min−1 to 260 °C,5 °C min−1 to 300 °C and held for 4 min. PCBs were monitored inselective ionmonitoringmode (EI-SIM) atmasses of [M]+ and [M+2]+

for mono- to tetra-CBs, [M+2]+ and [M+4]+ for penta- to nona-CBsand [M+4]+ and [M+6]+ for deca-CB. The instrumental set-up forPBDE analysis has been described previously (Sudaryanto et al.,2008b). HBCDs (α, β and γ isomers) were quantified by LC-MS/MSaccording to the methods described elsewhere (Isobe et al., 2007).Procedural blanks were analysed simultaneously with samples tocheck for interferences and contamination. Detection limits werecalculated as three times the procedural blank, and were in the rangeof 0.01–0.05 ng g−1 lipid wt. for all target compounds. Recoveries of13C-labelled surrogates were in the range of 57%–107% for PCBs, 63%–110% for PBDEs and 84%–113% for HBCDs. The analysis of humanbreast milk described above followed our common procedureemployed for animal tissues. For quality assurance and control, ourlaboratory participated in an intercalibration exercise on BFRs usingthe blubber of a marine animal as the referencematerial and our datawere in good agreement with those reported by other laboratories

ai (n=4) Trang Minh (n=11) Bui Dau (n=9)

(28.3) 18–26 (23.6) 24–35 (29.3)(46.0) 41–50 (45.5) 40–46 (44.0)5 (154.5) 150–160 (154.6) 150–155 (154.0).6 (19.3) 16.4–21.3 (19.1) 16.7–21.6 (19.1)3) 1–2 (1.55) 1–4 (2.2)6) 1.5–24 (12) 9.5–79 (34)ycler 55% recycler 55% recyclermer 45% housewife 45% others

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(Isobe et al., 2007). Concentrations were expressed on a lipid weightbasis unless otherwise specified.

2.4. Statistical analyses

The Wilcoxon rank sum test was used for assessing whether thecontaminant levels between groups were significantly different. Inthis analysis, non-detectable levels were set to zero. Principalcomponent analysis (PCA) was employed to categorise PCB andPBDE congeners according to their variation patterns. This analysisincluded only the congeners detected in at least 70% of the samples.The influence of socio-demographic parameters on the total concen-tration of each category was then analysed qualitatively usingmultiple linear regressions. The parameters used as independentvariables included: age, body mass index (BMI), total duration ofnursing, period of involvement in recycling activities and consump-tion rate of food from animal origin (total rate of meat, fish and dairyproducts, servings per week). Other location-specific factors wereassumed to be negligible and not considered. Parameters with a p-value of less than 0.05 were considered as having significantrelationship with contamination level. In these later two statisticalanalyses, non-detectable concentrations were set to half of thedetection limit and then all concentrations were log-transformed tobring the data distribution closer to normality. All calculations wereperformed using the statistical software package R version 2.9.0.

2.5. Risk assessment

The risk for infants exposed to contaminants in mother milk wasassessed using hazard quotients (HQs). An HQ is defined as the ratio ofthe estimated daily intake dose (DI) of the compound via breastfeed-ing to the correspondingmaximum acceptable oral dose for human, orreference dose (RfD). A value of HQ higher than 1 indicates potentialrisk. The DIs were calculated based on the assumption that an infant inaverage weighs 5 kg and consumes 700 gmothermilk daily (Oostdamet al., 1999). HQs of total PCBs, BDE-47, BDE-99, BDE-153 and total

Table 2Concentrations (ng g−1 lipid wt.) of major PCB congeners, PBDE congeners and HBCD isom

Compound Hanoi Dong Mai Trang

Median Range Median Range Medi

CB-28 1.1 0.42–7.6 5.6 1.0–34 2.0CB-74 2.8 1.3–6.0 5.9 1.2–15 2.7CB-99 2.9 1.2–7.3 2.5 0.88–4.6 2.1CB-118 4.8 2.0–13 3.5 1.2–8.3 3.3CB-138 9.7 3.8–17 4.0 2.1–11 5.8CB-153 8.2 3.8–16 3.5 1.7–9.0 5.7CB-180 3.7 1.9–5.5 1.0 0.51–3.5 1.8ΣPCBs 46 20–100 50 11–69 33BDE-15 0.040 0.014–0.073 0.011 0.010–0.032 0.030BDE-28 0.029 0.017–0.067 0.010 n.d.–0.044 0.074BDE-47 0.13 0.070–0.25 0.097 0.041–0.20 0.40BDE-99 0.057 n.d.–0.12 n.d. n.d.–0.028 0.11BDE-100 0.040 n.d.–0.10 n.d. n.d. 0.082BDE-153 0.098 0.062–0.14 0.10 0.061–0.25 0.40BDE-154 n.d. n.d.–0.037 n.d. n.d. 0.021BDE-183 0.029 n.d.–0.038 0.050 0.029–0.11 0.13BDE-196 0.010 n.d.–0.015 0.010 n.d.–0.018 0.036BDE-197 0.045 0.016–0.11 0.046 0.026–0.14 0.26BDE-206 n.d. n.d.–0.027 0.024 n.d.–0.10 0.05BDE-207 0.025 n.d.–0.057 0.030 0.011–0.11 0.10BDE-209 n.d. n.d. 0.17 0.069–0.50 0.42ΣPBDEs 0.57 0.24–0.8 0.73 0.26–1.1 2.3a

α-HBCD 0.33 0.066–1.4 0.43 0.11–0.97 0.38β-HBCD n.d. n.d. n.d. n.d. n.dγ-HBCD n.d. n.d.–0.13 n.d. n.d. n.d.ΣHBCDs 0.33 0.070–1.4 0.42 0.11–0.97 0.38

n.d.: not detected.a Significantly different from reference site (p<0.05).

HBCDs were calculated using RfD values of 1 (Oostdam et al., 1999),0.1, 0.1, 0.2 (EPA, 2008) and 0.2 µg kg−1 day−1 (European ChemicalsBureau, 2007), respectively.

3. Results

PCBs, PBDEs and HBCDs were detected in all the samples analysed(Table 2). In terms of total concentrations, PCBs were more abundantthan PBDEs and HBCDs by one order ofmagnitude or higher inmajorityof the samples. However, PBDEsweremore abundant than PCBs in threedonors who were involved in the recycling of e-waste in BD.

Total PCB levels were statistically comparable among locations butsignificant differences were observed with individual PCB congeners.The residents of the three recycling sites had statistically lower(p<0.05) levels of high-chlorinated congeners such as CB-138, -153and -180 but somewhat higher levels of tri- and tetra-chlorinatedcongeners (tri- and tetra-CBs) than those of the urban reference site.CB-28 was detected at significantly higher (p<0.05) levels in TM andBD (recyclers only) than in HN, and the highest levels of CB-28 andCB-74 were found in battery recyclers from DM. In each recycling site,the total levels of tri- and tetra-CBs were higher in the recycler groupthan in the non-recycler group, with the median being 30 vs 10, 6.7 vs4.9 and 5.0 vs 2.8 ng g−1 lipid wt. in DM, TM and BD, respectively.However, these differences were not statically significant (p>0.05),probably due to the limited number of samples. The preferentialaccumulation of these low-chlorinated biphenyls in the recycling sitesresulted in distinctive PCB congener profiles. As seen in Fig. 1, theprofile in the reference site followed the order of CB-138>CB-153>CB-118>CB-180>CB-99>CB-74>CB-28 whereas in TM andBD, CB-28 and CB-74 were as abundant as CB-99 and more than CB-180. In DM, the battery recycling site, CB-28 and CB-74 were thedominant congeners. Based on the PCA results PCB congeners weredivided into three categories (Fig. 2): (a) high-chlorinated PCBs(HighCB), including hepta to deca congeners and two hexa congeners(CB-138 and CB-153), aligned with the first principal component(PC1) which accounted for 57% of the total variance; (b) low-

ers in human breast milk collected from Hanoi and Vietnamese e-waste recycling sites.

Minh Bui Dau non-recyclers Bui Dau recyclers

an Range Median Range Median Range

0.72–10 0.85 0.42–14 1.9 1.5–140.42–7.6 1.6 0.56–3.7 2.7 1.6–8.60.60–4.3 1.7 0.60–2.0 2.8 1.9–3.61.0–6.9 2.8 1.0–3.3 4 3.6–5.61.9–11 4.8 1.7–6.0 5.5 4.6–6.71.8–11 3.6 1.5–5.2 4.6 3.6–5.60.71–4.3 1.4 0.50–2.1 1.6 1.3–1.711–73 24a 8.4–28 34 28–590.010–0.34 0.057 0.022–0.075 0.35 0.16–1.50.024–1.0 0.21 0.13–0.27 0.96 0.82–8.20.11–1.8 0.81 0.63–1.0 4.8 3.5–320.032–0.51 0.38 0.22–0.56 3.2 2.2–150.022–0.21 0.13 0.083–1.6 0.80 0.54–3.10.021–1.5 0.65 0.27–1.0 4.4 2.1–23n.d.–0.069 n.d. n.d.–0.035 0.39 0.27–2.10.022–1.2 0.14 0.053–0.22 1.2 0.49–2.7n.d.–0.14 0.037 0.027–0.056 0.59 0.25–5.10.032–0.78 0.47 0.17–0.61 7.5 3.1–290.012–0.23 0.014 n.d.–0.03 0.26 0.16–4.50.041–0.41 0.15 0.10–0.18 3.5 1.3–510.12–7.3 0.11 n.d.–0.16 4.1 0.87–960.55–13 3.2a 2.0–4.0 84a 20–2500.12–3.3 0.36 0.29–1.2 1.9 1.4–7.5n.d.–0.051 n.d. n.d. n.d. n.d.n.d.–0.27 n.d. n.d. 0.045 n.d.–0.0990.11–3.3 0.36 0.29–1.2 2.0a 1.4–7.6

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chlorinated PCBs (LowCB), consisting of mainly tri and tetracongeners, aligned with PC2 (17% of variance); and (c) others(MediumCB), mostly penta and a few hexa congeners including CB-99, -101, -118, -128, etc., contributing to both PCs.

PBDE levels in the battery recycling site DM were comparable withthose in the reference site HN whereas the levels in the two e-wastedismantling sites, TM and BD, were statistically higher (Table 2). In TM,the recycler and non-recycler groups had similar levels of total PBDEs,with anoverallmedianhigher than in the reference groupbya factor of 4.In BD, although the levels in the non-recycler group were onlycomparable to those in TM, the recycler group had the highest PBDElevels of all donors, approximately two orders of magnitude higher thanthose in the residents of HN. In the reference site, BDE-47 and BDE-153

Fig. 2. PCA loading plot of individual congeners of PCBs (left) and PBDEs

were the dominant PBDE congeners whereas BDE-209 was at non-detectable levels (Fig. 1). BDE-209 was detected in most of the samplescollected from the recycling sites with varying proportions up to 50%.Octa to nona congeners were also observed at higher percentages. BDE-197 and -207 were prominent in samples from recyclers living in BD,with levels comparable to BDE-47. PCA of PBDE congeners indicated thatthese compounds couldbe considered as a single category because86%ofthe variance could be represented by PC1 (Fig. 2), suggesting a highdegree of correlation among congeners with the exception of BDE-209,main contributor to PC2 (only 7.4% of the variance).

HBCDs levels were not statistically different among residents of HN,DM and TM (both recyclers and non-recyclers) and BD (non-recyclers).Recyclers from BD had significantly higher levels than the other groups,

(right). Numbers represent IUPAC numbers of PCB/PBDE congeners.

Table 3Coefficients (β) and p-values of socio-demographic parameters in linear models of contaminant concentrations.

Parameters LowCB MediumCB HighCB PBDEs HBCDs

β p β p β p β p β p

Age −0.028 0.19 −0.015 0.23 −0.007 0.51 0.005 0.88 −0.020 0.45BMI 0.062 0.36 0.046 0.09 0.023 0.22 −0.073 0.25 0.051 0.25Nursing time 0.008 0.11 −0.002 0.49 −0.0074 0.007 0.013 0.12 0.009 0.13Recyclinga 0.145 0.009 0.076 0.022 0.061 0.34 0.180 0.029 0.101 0.13Dietb 0.008 0.85 0.070 0.013 0.080 0.002 −0.037 0.64 0.003 0.96

R2 p R2 p R2 p R2 p R2 p

Model 0.40 0.013 0.37 0.023 0.48 0.002 0.38 0.018 0.24 0.17

a Period of involvement in recycling activities (years).b Consumption rate of food from animal origin (total rate for meat, fish and dairy products, servings per week).

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with a 6-fold difference compared with the reference group (Table 2).α-HBCD was the dominant isomer in all the samples, accounting formore than 90% of the total HBCD levels. γ-HBCD was detected in eightsampleswith a proportion of less than 10% and β-HBCDwas detected inonly one sample.

Results from the fitting of chemical concentrations to multiplelinear regression models of socio-demographic parameters (Table 3)showed that LowCB and PBDEs were associated only with involve-ment period in recycling activities, HighCB correlated positively withconsumption of food from animal origin but negatively with nursingtime whereas MediumCB had positive associations with both foodconsumption and recycling activities. Age and BMI did not show anysignificant influence on contaminant concentrations.

4. Discussion

4.1. Contamination levels

The similarity in PCB levels in the three Vietnamese e-wasterecycling sites as also seen in the reference site indicates that the

Table 4Comparison of PCBs and BFRs in human breast milk from Viet Nam with other countries.

Country Survey year PCBs PBD

Asian developing countriesChina 2003–2005 206

20042007

India 2002–2003 34

Indonesia 2001–2003 27Philippines 2004 60Vietnam (HN) 2007 46Vietnam (DM) 2007 51Vietnam (TM) 2007 33Vietnam (BD non-recylers) 2007 28Vietnam (BD recyclers) 2007 34

Other countriesJapan 2004 65

2006Belgium 2006 123Norway 2000–2002 165Russia 2002 175Spain 2003–2004 111

2006–2007Sweden 2002–2003 111United Kingdom 2001–2003 180United States 2002–2003 126

Concentrations are given as median if available (or arithmetic mean otherwise) and expresa Mono- to hepta-BDEs only.b Mono- to hexa-BDEs only.c Pooled values.

former were notmajor sources of PCBs. Total PCB levels in Vietnamesehuman breast milk were in comparable ranges with those reported inother Asian developing countries and lower than in developed nations(Table 4). The levels observed in this study were similar to the serumPCB levels in the residents of Guiyu (median 52 ng g−1 lipid wt.), thelargest recycling site of electronic waste in China, reported by Bi et al.(2007). These authors also did not find any significant differencebetween the exposed and the reference populations. Thus e-wasterelated PCB contamination is believed to involve old electric materials,especially transformers, rather than electronic waste. The case ofLuqiao, the largest Chinese disassembly site of electrical waste, is anexample where very high PCB levels in human breast milk associatedwith e-waste recycling were reported (median 359 ng g−1 lipid wt.,Zhao et al., 2007). The absence of substantial PCB contaminationsuggests that in the Vietnamese recycling sites, the occurrence ofwaste materials containing PCBsmay be uncommon and the recyclingof these materials is of limited scale.

Significant exposure to PBDEs was observed in the two e-wastedismantling sites, TM and BD, especially in BD recyclers. Comparedwith the levels reported by other studies, the PBDE levels in the

Es HBCDs References

7.1 0.86 Zhao et al. (2007)Sudaryanto et al. (2008b)Shi et al. (2009)

0.6a Subramanian et al. (2007),Sudaryanto et al. (2005)

1.5 Sudaryanto et al. (2008a)3.8 0.62 Malarvannan et al. (2009)0.57 0.33 This study0.73 0.42 This study2.3 0.38 This study3.2 0.36 This study

84 2.0 This study

1.54 1.4–4.0c Inoue et al. (2006)Kakimoto et al. (2008)

2.01 1.5 Colles et al. (2008)3.19 0.13 Polder et al. (2008b)0.96 0.62 Polder et al. (2008a)6.1 27 Bordajandi et al. (2008),

Gómara et al. (2007),Eljarrat et al. (2009)

2.93a 0.35 Lignell et al. (2003)6.3b Kalantzi et al. (2004)

50.4 0.5 Ryan et al. (2006), She et al. (2007)

sed in nanogram per gram lipid wt.

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reference group in this study (HN) were among the lowest in theworld (Table 4), consistent with the findings of Schecter et al. (2004).Levels in TM and BD non-recyclers were higher in Indonesia and Japanand close to those in European countries whereas levels in BDrecyclers were in the same range with American levels which are thehighest reported among non-occupationally exposed populations.The differences in waste materials, workload and processing methodsmay contribute to the variation of PBDE contamination levels in theVietnamese recycling sites. For instance, PBDEs may be minor con-taminants in waste batteries as suggested by the low levels accu-mulated in the battery recyclers in DM. On the other hand, theelevated levels in recyclers from BD may be the result of processinglarge amounts of waste materials with high PBDE contents usingmethods which facilitate the release of these contaminants from thewaste matrices, such as burning and other thermal processes. It is alsoremarkable that in BD recyclers, the PBDEs levels exceeded those ofPCBs, despite the long legacy of the latter compounds. This unusualfeature (comparison in Table 4) has so far been observed only in caseof uncontrolled e-waste recycling (Bi et al., 2007). It clearly indicatesan extensive exposure to PBDEs with different sources from those oflegacy persistent organic pollutants (POPs); nevertheless the highestPBDE levels in breast milk in this study were still lower than those inserum of Chinese e-waste dismantling workers from Guiyu (median600 ng g−1 lipid wt., Bi et al., 2007) by an order of magnitude. This largedifference in lipid weight-normalised concentrations, albeit in twoseparate human matrices, again infers that Vietnamese recycling sitesare still less contaminated in terms of PBDEs than their Chinese counter-parts, probably on account of a smaller scale of e-waste processing.

Although information on HBCDs in human matrices is still limited,available data indicate that the accumulation levels of HBCDs inhuman breast milk from Asia, USA and several European countries arevery low (<1 ng g−1 lipid wt., Table 4). The HBCD levels in HN, DMand TM observed in this study also fell within this range, suggestingthat products containing HBCDs may be scarce in Viet Nam and alsouncommon in the e-waste. In contrast, the contamination levels werereported to be somewhat higher in Japan and very high in Spain(Table 4), reflecting an extensive usage of HBCDs in Japan and someEuropean countries (Watanabe and Sakai, 2003). InVietnamese e-wasterecycling sites, exposure towastematerials containingHBCDs appearedto be limited to recyclers from BD, coincidentally the group mostexposed to PBDEs. The HBCD levels in this groupwere comparable withthose in Japanesewomen;nevertheless these exposure levels associatedwith e-waste recyclingwere stillmuch lower than thenon-occupationalexposure levels reported in Spain.

4.2. Accumulation patterns

Higher levels of tri- and tetra-CBs in the recycling sites indicate aspecific exposure in e-waste recycling processes. This is furthersupported by a significant positive relationship between LowCB leveland period of involvement time in recycling activities (Table 3). Thesource of these congeners may be old electric devices such ascapacitors and small transformers which contain PCBs as heat transferand dielectric fluids. Several PCB technical mixtures such as Aroclor1016, 1242 or Kaneclor 300 contain principally congeners with lowdegrees of chlorination (Takasuga et al., 2006). Moreover, low-chlorinated biphenyls from e-waste can be more accessible to humandue to their relatively higher volatility (Bamford et al., 2000). Thisexposure source may explain the highest levels of tri- and tetra-CBsfound in DM, a site recycling exclusively electrical waste.

The elevated relative concentrations of octa- to deca-BDEs in therecycling sites were the distinctive feature compared with the PBDEprofile in HN which was dominated by lower-brominated congenerssuch as BDE-47 and BDE-153. The latter pattern seems to be commonin human breast milk frommany countries in Asia (Inoue et al., 2006;Sudaryanto et al., 2008a), Europe (Polder et al., 2008a) and North

America (She et al., 2007). There are several plausible explanationsfor the preferential accumulation of BDE-47 and BDE-153 in human:they are major constituents of the PentaBDE technical mixtures (LaGuardia et al., 2006), have relatively good bioavailability (Hakk andLetcher, 2003) and strong bioaccumulation features (Burreau et al.,2006) and can be metabolites of higher-brominated congeners(Stapleton et al., 2004). Therefore secondary exposure via diet maybe the major pathway of BDE-47 and BDE-153. On the other hand,high-brominated BDEs, notably BDE-209 are poorly biomagnifiedthrough food webs (Burreau et al., 2006). BDE-209 also has a very lowassimilation rate (<1%) and a fast clearance rate in mammals (Hakkand Letcher, 2003). Thus accumulation of high-brominated BDEs isoften attributed to a sustained exposure to Octa and DecaBDEtechnical mixtures at elevated levels, especially in an occupationalcontext such as the case of rubber and cablemanufacturingworkers inSweden (Thuresson et al., 2005) or e-waste recycling workers inChina (Bi et al., 2007). Therefore the presence of octa- to deca-BDEs inbreast milk of the mothers in Vietnamese e-waste recycling sitescould be an indication of primary exposure to Octa and DecaBDEtechnical mixtures from e-waste. The large variation in relative con-centrations of these congeners even within the same group suggeststhat either human exposure to higher-brominated BDEs may varywith different microenvironments depending probably on thecomposition of the flame retardants contained in waste materials, orthe toxicokinetics of these compounds may be different in individualdonors.

4.3. Exposure pathways

As PBDE levels did not correlate with HighCB levels (Pearson's r=−0.012, p=0.95), the two groups of compounds may have differentexposure sources/pathways. In case of HighCB, the main pathway islikely to be dietary intake, evidenced by a positive association withconsumption of food fromanimal origin (Diet parameter, Table 3). Thisis often the case with legacy POPs such as high-chlorinated PCBs thathave been accumulated in biota, especially fatty tissues of animals,during their extensive release in the past. A dietary exposure alsoexplains the higher accumulation in the urban population that hadricher diets than the residents of the recycling sites. On the other hand,exposure to PBDEs and LowCB seems to be mainly non-dietary andrelated to the recycling of e-waste, as indicated by a single significantpositive association with involvement time in recycling activities(Recycling parameter, Table 3). This occupational exposure may occurthrough accidental ingestion/inhalation of particulate matters gener-ated during activities such as dismantling, shredding or thermal treat-ment of e-waste. In another case of uncontrolled e-waste recycling,elevated concentrations of air particles and extremely high concen-trations of air particle-bound PBDEs have indeed been reported (Wonget al., 2007). In this study, dietary intake did not appear to be animportant factor contributing to PBDE levels, partly because the mainsupplies of food fromanimal originwere not produced on site and thusnot directly contaminated by the recycling activities.

The exposure to HBCDs may occur in a similar fashion to PBDEs astheir levels correlatedwith each other (Pearson's r=0.72, p<0.0001).HBCD levels also have a positive association with recycling acti-vities, though not statistically significant (p=0.13, Table 3). In caseof PCB congeners in the MediumCB category, the exposure path-ways may be both dietary and non-dietary through occupationalcontact with e-waste, as suggested by the positive associationswith Diet and Recycling parameters (p=0.013 and 0.022, respec-tively, Table 3).

4.4. Depuration by lactation

Another noteworthy detail is the difference in depuration featureof the target compounds. In the literature, legacy POPs such as PCBs

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tend to have lower levels in multiparae (mothers having given birthtwice or more) than in primiparae (first-time mothers) because asignificant portion of the mother's body burden is transferred to thechild during nursing, as remarked by Tanabe and Kunisue (2007) in areview on POPs in humanmilk. However, in the case of emerging POPssuch as BFRs, the decrease in the mother's burden by lactation wasreported to be not appreciable (Hooper et al., 2007; Schecter et al.,2003; Sudaryanto et al., 2008a) because recent intake may compen-sate the loss via breastfeeding. In this study, BFR levels also did notshow any negative correlation with nursing time, unlike HighCB,indicating that human exposure to BFRs is continuous and that theintake rate may be comparable to the rate of depuration via lactation.

4.5. Infant health risk

As shown in Fig. 3, the health risk for infants exposed to the targetcontaminants via breastfeeding in general may not be serious sincethe majority of HQ values are below 1, albeit the HQs of PCBs arerelatively high (>0.1) in most cases. Thus PCB accumulation inVietnamese human milk, as a consequence of a long usage history(Minh et al., 2008) rather than e-waste recycling, should still beconsidered with respect to safe consumption by infants. HQ values ofBFRs are generally lower than 0.1, with the exception of recyclers inBD. This group has high HQs related to PBDEs, with several valuesclose to or exceeding 1, indicating potential health risk for theirchildren. The health effects for the infant in the event of daily intakedose of PBDEs exceeding the RfDs, which were derived from studieson neurobehavioural developmental toxicities (EPA, 2008), mayinclude altered motor behaviour, decreased habituation capability,decreased learning/memory ability or more serious effects. More indepth epidemiological studies are necessary to assess the effects ofPBDE exposure on the development of children in these recyclingsites.

5. Conclusions

The present study found a significant accumulation of PBDEs inbreast milk of women living in two Vietnamese e-waste dismantlingsites, possibly through non-dietary intake by accidental ingestion/inhalation of dust. The highest PBDE levels were found in recyclers

Fig. 3. Hazard quotients of total PCBs, BDE-47, BDE-99, BDE-153 and total HBCDscalculated for breastfeeding infants.

from the village Bui Dau, higher than the reference levels by twoorders of magnitude and comparable to the highest levels reported inindustrialised countries. PBDEs levels in these recyclers also exceededthose of legacy POPs such as PCBs. These Vietnamese e-waste re-cycling sites may be less contaminated than their Chinese counter-parts in terms of PCBs and PBDEs; nevertheless the levels of BDE-47and BDE-99 in breastmilk of somemothers occupationally involved inrecycling were sufficiently high to be considered unsafe for breast-feeding infants. Thus it is clear that the contamination caused by therecycling of e-waste should be mitigated to reduce human exposureto PBDEs and also to a multitude of other toxic substances releasedduring e-waste recycling activities such as heavy metals, dioxin-likecompounds, polyaromatic hydrocarbons, etc. In order to have a morecomplete understanding of the impact of e-waste recycling in thestudy locations, these contaminants should be considered in futureworks and dust may provide a good sample matrix for assessment ofhuman exposure.

Acknowledgements

The authors thankMr Bui Hong Nhat for coordinating the samplingsurvey. This study was partly supported by the grants-in-aid forscientific research (S) (no. 20221003) from Japan Society for thePromotion of Science (JSPS), the global environment research fund(RF-064) and the waste management research grants (K2062, K2129and K2121) from the Ministry of the Environment, Japan, and grantsfrom global COE program from the Japanese Ministry of Education,Culture, Sports, Science and Technology (MEXT).

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